The Capsid Proteins of a Large, Icosahedral dsDNA Virus

Journal of Molecular Biology

Volumn 385, Issue 4, 2009, Pages 1287-1299

  Yan, Xiaodong ^a,b   Yu, Zeyun ^c   Zhang, Ping ^d   Battisti, Anthony J ^d   Holdaway, Heather A ^d   Chipman, Paul R ^d   Bajaj, Chandrajit ^c   Bergoin, Max ^e   Rossmann, Michael G ^d   Baker, Timothy S ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SECTION OF MOLECULAR BIOLOGY   (United States)

^c University of Texas at Austin   (United States)

^d PURDUE UNIVERSITY   (United States)

^e UNIV MONTPELLIER   (France)

Author keywords

3D image reconstruction; cryoelectron microscopy; enveloped virus; large DNA virus; minor capsid proteins

Indexed keywords

CAPSID PROTEIN; DOUBLE STRANDED DNA; MEMBRANE PROTEIN; PROTEIN P50; UNCLASSIFIED DRUG; VP54 MAJOR CAPSID PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CHILO IRIDESCENT VIRUS; CHLORELLA VIRUS; CROSS LINKING; CRYOELECTRON MICROSCOPY; DNA VIRUS; GENOME; IMAGE RECONSTRUCTION; LIPID MEMBRANE; NONHUMAN; PARAMECIUM BURSARIA CHLORELLA VIRUS; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN STABILITY; SEQUENCE HOMOLOGY; THREE DIMENSIONAL IMAGING; VIRUS MORPHOLOGY;

DNA VIRUSES; HEXAPODA; INVERTEBRATE IRIDESCENT VIRUS 6; MIRIDAE; PARAMECIUM BURSARIA CHLORELLA VIRUS 1;

EID: 58149344970     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.11.002     Document Type: Article

References (51)

1. Iyer L.M., Balaji S., Koonin E.V., and Aravind L. Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Virus Res. 117 (2006) 156-184
2. Suzan-Monti M., La Scola B., Barrassi L., Espinosa L., and Raoult D. Ultrastructural characterization of the giant volcano-like virus factory of Acanthamoeba polyphaga Mimivirus. PLoS ONE 2 (2007) e328
3. Iyer L.M., Aravind L., and Koonin E.V. Common origin of four diverse families of large eukaryotic DNA viruses. J. Virol. 75 (2001) 11720-11734
4. Van Etten J.L., Graves M.V., Müller D.G., Boland W., and Delaroque N. Phycodnaviridae-large DNA algal viruses. Arch. Virol. 147 (2002) 1479-1516
5. La Scola B., Audic S., Robert C., Jungang L., de Lamballerie X., Drancourt M., et al. A giant virus in amoebae. Science 299 (2003) 2033
6. Zauberman N., Mutsafi Y., Halevy D.B., Shimoni E., Klein E., Xiao C., et al. Distinct DNA exit and packaging portals in the virus Acanthamoeba polyphaga mimivirus. PLoS Biol. 6 (2008) 1104-1114
7. Yan X., Chipman P.R., Castberg T., Bratbak G., and Baker T.S. The marine algal virus PpV01 has an icosahedral capsid with T = 219 quasisymmetry. J. Virol. 79 (2005) 9236-9243
8. Yan X., Olson N.H., Van Etten J.L., Bergoin M., Rossmann M.G., and Baker T.S. Structure and assembly of large lipid-containing dsDNA viruses. Nat. Struct. Biol. 7 (2000) 101-103
9. Nandhagopal N., Simpson A.A., Gurnon J.R., Yan X., Baker T.S., Graves M.V., et al. The structure and evolution of the major capsid protein of a large, lipid-containing DNA virus. Proc. Natl Acad. Sci. USA 99 (2002) 14758-14763
10. Simpson A.A., Nandhagopal N., Van Etten J.L., and Rossmann M.G. Structural analyses of Phycodnaviridae and Iridoviridae. Acta Crystallogr., Sect. D: Biol. Crystallogr. 59 (2003) 2053-2059
11. Wrigley N.G. An electron microscope study of the structure of Sericesthis iridescent virus. J. Gen. Virol. 5 (1969) 123-134
12. Caspar D.L., and Klug A. Physical principles in the construction of regular viruses. Cold Spring Harbor Symp. Quant. Biol. 27 (1962) 1-24
13. Rossmann M.G., and Johnson J.E. Icosahedral RNA virus structure. Annu. Rev. Biochem. 58 (1989) 533-573
14. Fabry C.M., Rosa-Calatrava M., Conway J.F., Zubieta C., Cusack S., Ruigrok R.W., and Schoehn G. A quasi-atomic model of human adenovirus type 5 capsid. EMBO J. 24 (2005) 1645-1654
15. Benson S.D., Bamford J.K.H., Bamford D.H., and Burnett R.M. Viral evolution revealed by bacteriophage PRD1 and human adenovirus coat protein structures. Cell 98 (1999) 825-833
16. Abrescia N.G.A., Cockburn J.J.B., Grimes J.M., Sutton G.C., Diprose J.M., Butcher S.J., et al. Insights into assembly from structural analysis of bacteriophage PRD1. Nature (London) 432 (2004) 68-74
17. Abrescia N.G.A., Grimes J.M., Kivelä H.M., Assenberg R., Sutton G.C., Butcher S.J., et al. Insights into virus evolution and membrane biogenesis from the structure of the marine lipid-containing bacteriophage PM2. Mol. Cell 31 (2008) 749-761
18. Laurinmaki P.A., Huiskonen J.T., Bamford D.H., and Butcher S.J. Membrane proteins modulate the bilayer curvature in the bacterial virus Bam35. Structure 13 (2005) 1819-1828
19. Lin T., Chen Z., Usha R., Stauffacher C.V., Dai J.-B., Schmidt T., and Johnson J.E. The refined crystal structure of cowpea mosaic virus at 2.8 Å resolution. Virology 265 (1999) 20-34
20. Benson S.D., Bamford J.K., Bamford D.H., and Burnett R.M. Does common architecture reveal a viral lineage spanning all three domains of life?. Mol. Cell 16 (2004) 673-685
21. Tsao J., Chapman M.S., Agbandje M., Keller W., Smith K., Wu H., et al. The three-dimensional structure of canine parvovirus and its functional implications. Science 251 (1991) 1456-1464
22. McKenna R., Xia D., Willingmann P., Ilag L.L., Krishnaswamy S., Rossmann M.G., et al. Atomic structure of single-stranded DNA bacteriophage phiX174 and its functional implications. Nature (London) 355 (1992) 137-143
23. Devauchelle G., Attias J., Monnier C., Barray S., Cerutti M., Guerillon J., and Orangebalange N. Chilo iridescent virus. Curr. Top. Microbiol. Immunol. 116 (1985) 37-48
24. Jakob N.J., Muller K., Bahr U., and Darai G. Analysis of the first complete DNA sequence of an invertebrate iridovirus: coding strategy of the genome of Chilo iridescent virus. Virology 286 (2001) 182-196
25. Goorha R., and Murti K.G. The genome of frog virus 3, an animal DNA virus, is circularly permuted and terminally redundant. Proc. Natl Acad. Sci. USA 79 (1982) 248-252
26. Darai G., Anders K., Koch H.G., Delius H., Gelderblom H., Samalecos C., and Flugel R.M. Analysis of the genome of fish lymphocystis disease virus isolated directly from epidermal tumours of pleuronectes. Virology 126 (1983) 466-479
27. Miller E.S., Kutter E., Mosig G., Arisaka F., Kunisawa T., and Ruger W. Bacteriophage T4 genome. Microbiol. Mol. Biol. Rev. 67 (2003) 86-156
28. Schnitzler P., Soltau J.B., Fischer M., Reisner H., Scholz J., Delius H., and Darai G. Molecular cloning and physical mapping of the genome of insect iridescent virus type 6: further evidence for circular permutation of the viral genome. Virology 160 (1987) 66-74
29. Cerutti M., and Devauchelle G. Characterization and localization of CIV polypeptides. Virology 145 (1985) 123-131
30. Stohwasser R., Raab K., Schnitzler P., Janssen W., and Darai G. Identification of the gene encoding the major capsid protein of insect iridescent virus type 6 by polymerase chain reaction. J. Gen. Virol. 74 (1993) 873-879
31. Balange-Orange N., and Devauchelle G. Lipid composition of an iridescent virus type 6 (CIV). Arch. Virol. 73 (1982) 363-367
32. Bamford D.H., Grimes J.M., and Stuart D.I. What does structure tell us about virus evolution?. Curr. Opin. Struct. Biol. 15 (2005) 655-663
33. Jäälinoja H.T., Roine E., Laurinmaki P., Kivela H.M., Bamford D.H., and Butcher S.J. Structure and host-cell interaction of SH1, a membrane-containing, halophilic euryarchaeal virus. Proc. Natl Acad. Sci. USA 105 (2008) 8008-8013
34. Harauz G., and van Heel M. Exact filters for general geometry three dimensional reconstruction. Optik 73 (1986) 146-156
35. Yan X., Sinkovits R.S., and Baker T.S. AUTO3DEM-an automated and high throughput program for image reconstruction of icosahedral particles. J. Struct. Biol. 157 (2007) 73-82
36. Fokine A., Leiman P.G., Shneider M.M., Ahvazi B., Boeshans K.M., Steven A.C., et al. Structural and functional similarities between the capsid proteins of bacteriophages T4 and HK97 point to a common ancestry. Proc. Natl Acad. Sci. USA 102 (2005) 7163-7168
37. Khayat R., Tang L., Larson E.T., Lawrence C.M., Young M., and Johnson J.E. Structure of an archaeal virus capsid protein reveals a common ancestry to eukaryotic and bacterial viruses. Proc. Natl Acad. Sci. USA 102 (2005) 18944-18949
38. Cusack S. Adenovirus complex structures. Curr. Opin. Struct. Biol. 15 (2005) 237-243
39. Zhang Y., Corver J., Chipman P.R., Zhang W., Pletnev S.V., Sedlak D., et al. Structures of immature flavivirus particles. EMBO J. 22 (2003) 2604-2613
40. Wriggers W., Milligan R.A., and McCammon J.A. Situs: a package for docking crystal structures into low-resolution maps from electron microscopy. J. Struct. Biol. 125 (1999) 185-195
41. Rossmann M.G., Bernal R., and Pletnev S.V. Combining electron microscopic with X-ray crystallographic structures. J. Struct. Biol. 136 (2001) 190-200
42. Yu Z., and Bajaj C. Automatic ultrastructure segmentation of reconstructed cryoEM maps of icosahedral viruses. IEEE Trans. Image Process. 14 (2005) 1324-1337
43. San Martin C., Huiskonen J.T., Bamford J.K., Butcher S.J., Fuller S.D., Bamford D.H., and Burnett R.M. Minor proteins, mobile arms and membrane-capsid interactions in the bacteriophage PRD1 capsid. Nat. Struct. Biol. 9 (2002) 756-763
44. Huiskonen J.T., Kivela H.M., Bamford D.H., and Butcher S.J. The PM2 virion has a novel organization with an internal membrane and pentameric receptor binding spikes. Nat. Struct. Mol. Biol. 11 (2004) 850-856
45. Martins M.D., Cavalcanti de Araujo V., Raitz R., and Soares de Araujo N. Expression of cytoskeletal proteins in developing human minor salivary glands. Eur. J. Oral Sci. 110 (2002) 316-321
46. Saban S.D., Silvestry M., Nemerow G.R., and Stewart P.L. Visualization of alpha-helices in a 6-angstrom resolution cryoelectron microscopy structure of adenovirus allows refinement of capsid protein assignments. J. Virol. 80 (2006) 12049-12059
47. Baker T.S., and Cheng R.H. A model-based approach for determining orientations of biological macromolecules imaged by cryoelectron microscopy. J. Struct. Biol. 116 (1996) 120-130
48. Jones T.A., Zou J.Y., Cowan S.W., and Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47 (1991) 110-119
49. Yu, Z. & Bajaj, C. (2008). Computational approaches for automatic structural analysis of large bio-molecular complexes. IEEE/ACM Trans. Comput. Biol. Bioinfor., in press. doi:10.1109/TCBB.2007.70226.
50. Kleywegt G.J., and Jones T.A. Software for handling macromolecular envelopes. Acta Crystallogr., Sect. D: Biol. Crystallogr. 55 (1999) 941-944
51. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., and Ferrin T.E. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004) 1605-1612